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Ecology, 91(12), 2010, pp. 3609–3619 Ó 2010 by the Ecological Society of America Climate change effects on an endemic-rich edaphic flora: resurveying Robert H. Whittaker’s Siskiyou sites (Oregon, USA) ELLEN I. DAMSCHEN,1,4 SUSAN HARRISON,2 AND JAMES B. GRACE3 1 Department of Biology, Washington University, St. Louis, Missouri 63130 USA Department of Environmental Science and Policy, University of California, Davis, California 95616 USA 3 U.S. Geological Survey, National Wetlands Research Center, 700 Cajundome Boulevard, Lafayette, Louisiana 70506 USA 2 Abstract. Species with relatively narrow niches, such as plants restricted (endemic) to particular soils, may be especially vulnerable to extinction under a changing climate due to the enhanced difficulty they face in migrating to suitable new sites. To test for community-level effects of climate change, and to compare such effects in a highly endemic-rich flora on unproductive serpentine soils vs. the flora of normal (diorite) soils, in 2007 we resampled as closely as possible 108 sites originally studied by ecologist Robert H. Whittaker from 1949 to 1951 in the Siskiyou Mountains of southern Oregon, USA. We found sharp declines in herb cover and richness on both serpentine and diorite soils. Declines were strongest in species of northern biogeographic affinity, species endemic to the region (in serpentine communities only), and species endemic to serpentine soils. Consistent with climatic warming, herb communities have shifted from 1949–1951 to 2007 to more closely resemble communities found on xeric (warm, dry) south-facing slopes. The changes found in the Siskiyou herb flora suggest that biotas rich in narrowly distributed endemics may be particularly susceptible to the effects of a warming climate. Key words: biodiversity; biogeographic affinity; climate change; edaphic; endemism; gradients; plant community; Robert H. Whittaker; serpentine; soil type; species distribution; topography. INTRODUCTION Earlier budburst and flowering (Menzel et al. 2006), upward shifts of montane floras (Beckage et al. 2008, Kelly and Goulden 2008, Lenoir et al. 2008) and faunas (Moritz et al. 2008), and local extinctions of populations at low elevations and latitudes (Parmesan et al. 1999, Parmesan and Yohe 2003) testify to the ever-growing evidence for biotic impacts of global warming. Forecasts of biotic change over the coming decades, derived by modeling current vs. future climatic envelopes of species, predict many global extinctions and dramatic reorganizations of natural communities (Thomas et al. 2004, Schwartz et al. 2006, Loarie et al. 2008). Yet one aspect of these forecasts may make them too optimistic: they assume that even without any dispersal species will at least survive in the geographic areas of overlap between their present and future climatic envelopes. However, this ignores other niche requirements that must be met in addition to climatic suitability. For example, plants confined to patchy outcrops of special soils such as serpentine or limestone might be expected to have far lower chances of successful migration to suitable sites than plants that are soil generalists (Van de Ven et al. Manuscript received 12 June 2009; revised 17 March 2010; accepted 7 April 2010. Corresponding Editor: K. D. Woods. 4 Present address: Department of Zoology, Birge Hall, University of Wisconsin, Madison, Wisconsin 53706 USA. E-mail: [email protected] 2007). Extinction risks may be just as high in these ‘‘edaphic island’’ endemics as in the better-known case of species confined to mountaintop ‘‘islands’’ (e.g., Pounds et al. 1999, Raxworthy et al. 2008). Few studies have examined the sensitivity of specialsoil floras to human-induced climate change or other widespread environmental alterations (but see Grime et al. 2000, 2008). Yet global biological diversity is greatly enhanced by edaphic endemics, such as the rich floras of limestone grasslands in southern Europe, dolomite glades in the Ozarks, shale barrens in Appalachia, or serpentine outcrops in the Mediterranean, Cuba, New Caledonia, and California (Anderson et al. 1999, Kruckeberg 2005). In California, one of the world’s botanical diversity hotspots (Myers et al. 2000, Stein et al. 2000), 612 of 1742 rare plants are associated with serpentine, limestone, volcanic outcrops, vernal pools, or other special substrates (Skinner and Pavlik 1994), and plants restricted to serpentine comprise .10% of species unique to the state even though serpentine is ,2% of its area (Kruckeberg 2005, Safford et al. 2005). Edaphic endemic plants have also been important subjects for evolutionary studies (Brady et al. 2005). Despite their naturally fragmented distributions, there are several possible reasons for optimism about the future of special-soil floras. One is that many of them are found in zones of mountain uplift (Anderson et al. 1999, Kruckeberg 2005), offering the hope of survival through local shifts in elevation or from south- to north-facing slopes (Loarie et al. 2009). Also, edaphic endemic species 3609 3610 ELLEN I. DAMSCHEN ET AL. may have suites of traits that render them relatively resistant to climate change (Grime et al. 2000, 2008, Theurillat and Guisan 2001). For example, greater drought tolerance in serpentine endemics is suggested by their often xeromorphic (small, thick, hairy) leaves, as well as some experimental evidence (Brady et al. 2005). In general, it may be that edaphic endemics tolerate nutrient-poor or excessively cation-rich (‘‘toxic’’) soils at the expense of having low maximal growth rates even when resources are abundant. Thus, some studies have suggested that floras on special soils will be less sensitive to altered temperature and water availability than those of more fertile soils (Grime et al. 2000, 2008, Theurillat and Guisan 2001). Also, other studies suggest that climate change may cause species to alter their habitat specificity through either ecological or evolutionary processes (Thomas et al. 2001, Davies et al. 2006); for example, species may become less restricted to serpentine in harsher, less-productive climates (Harrison et al. 2009). We tested the relative sensitivity of an edaphic endemic flora to climate change by resampling vegetation in the Siskiyou Mountains of southern Oregon and northern California at sites studied by ecologist Robert Whittaker from 1949 to 1951 (Whittaker 1960). Within a region of extraordinary plant diversity and endemism, Whittaker measured the effects of topography and soil parent material on plant community composition. Climatic warming has since been documented throughout the Pacific Northwest (Mote et al. 2003), including in Whittaker’s study region (;28C increase in mean summer temperatures from 1948 to 2007 in Medford, Oregon; NOAA 2009; see Appendix A). By resampling his sites 57 years later we can ask, first, whether community composition has shifted in the direction expected under a warming climate, second, whether the rich endemic flora on serpentine soil has been more or less susceptible to such a shift than the flora of normal soils; and third, whether local topography has provided a refuge for plant species in the face of climate change. METHODS Study system The Klamath-Siskiyou Mountains (California and Oregon, USA) are one of North America’s most significant hotspots of plant diversity and endemism, whose 3500 plant species include 131 species endemic to the region and ;700 close to their northern or southern range limits (Ricketts et al. 1999, Myers et al. 2000). Exceptional botanical richness in this region has been attributed to several factors: high topographic and geologic complexity; a central location between the Pacific Northwestern, Californian, and interior floras; and a consistently favorable climate that has permitted survival of plants from the mild and wet Tertiary (Axelrod 1958, Whittaker 1960, Coleman and Kruckeberg 1999). Ecology, Vol. 91, No. 12 The region includes North America’s largest exposure of serpentine or ultramafic (extremely high Mg and Fe) rock. The large area, great age (.50 million years), high rainfall, and topographic complexity of its ultramafic rocks combine to make it the continent’s leading location for edaphic endemism; of 246 plant taxa confined to serpentine in California, 97 are found here (Coleman and Kruckeberg 1999, Safford et al. 2005, Alexander et al. 2006, Harrison et al. 2006). From 400 to 700 m, serpentine soils support open woodland with Jeffrey pine (Pinus jeffreyi ), incense cedar (Calocedrus decurrens), and a rich herb understory. From 700 to 1200 m, there is a denser coniferous overstory (e.g., Douglas-fir, Pseudotsuga menziesii, western white pine, Pinus monticola) and a shrubby understory (e.g., huckleberry oak, Quercus vaccinifolia; shrub tanoak, Lithocarpus densiflorus var. echioides) (Whittaker 1960). Other substrates represented in Whittaker’s study included diorite, a sialic (high Si ) igneous rock similar to granite, and gabbro, a mafic (moderately high Mg and Fe) igneous rock with chemistry intermediate between diorite and serpentine. From 500 to 1200 m, diorite soils support typical vegetation for the region: closed forest dominated by Douglas-fir with scattered ponderosa pine (Pinus ponderosa), sugar pine (Pinus lambertiana), and broadleaved evergreens (tanoak; madrone, Arbutus menziesii; canyon live oak, Quercus chrysolepis); white fir (Abies concolor) increases in abundance with elevation (Whittaker 1960). Much of Whittaker’s study area was logged in the 1960s–1980s (Jules et al. 2008), but in our study we avoided logged sites. Other recent human impacts on the region’s vegetation include fire suppression since the early 20th century (Agee 1991, Skinner 1995). None of our sites were grazed by livestock, and exotic species were infrequent (see Results). Historic data collection Whittaker quantified plant communities along three gradients: elevation, soil type, and the local variation from cool north-facing to warm south-facing slopes that he called the ‘‘topographic moisture gradient’’ (TMG): a semi-quantitative spectrum from 1 to 10, where low values indicate communities on cool or ‘‘mesic’’ sites (e.g., mild to moderate north-facing slopes), and high values indicate communities on warm or ‘‘xeric’’ sites (e.g., steep south-facing slopes). He considered the TMG to be a product of multiple factors, including wind exposure, soil depth and chemistry, temperature, and moisture, and believed it could best be quantified using vegetation data. In the absence of computers, he sought simple methods to ordinate community samples along this gradient. His did this by subjectively choosing plots and assigning them to positions on the 10-point TMG scale, sampling their vegetation, and then using the frequencies of indicator species to refine the assignment of plots to December 2010 ENDEMIC-RICH FLORA AND CLIMATE CHANGE positions on the 10-point scale (Whittaker 1960). Sometimes, for unknown reasons, he used gradient lengths other than 10 (range 6–11). Also, he sometimes assigned multiple gradient scores to a single site. We standardized his topographic moisture scores to a gradient of 0–1 and averaged these to arrive at a single TMG score for each site. We found that these scores were correlated (r ¼ 0.51, P , 0.001) with estimated January insolation for each site, a function of slope and aspect (McCune 2007). As sites range from TMG scores of 0 to 1, some species (Whittaker’s ‘‘mesic indicators’’) consistently decrease and others (his ‘‘xeric indicators’’) consistently increase in abundance (Appendix B). Whittaker collected data from 290 plots on diorite soils, 55 plots on serpentine, and 51 plots on gabbro soils from June–August 1949–1951 (hereafter, 1950). Within each soil, he chose at least five plots representing each point on his 10-point scale, where a score of 1 was very mesic (usually along a ravine with flowing water), scores of 2–4 were progressively less mesic (usually north and northeast-facing or not very steep), 5–6 were intermediate (e.g., northwest or southeast slopes), and 7–10 were more xeric (e.g., a 10 being a steep south or southwest slope). On diorite, he repeated this arrangement for each of several elevational bands between 500 and 2000 m. He chose relatively homogeneous tree stands, avoided obvious disturbances and openings, and sampled near roads and trails for efficiency (Whittaker 1960, Westman and Peet 1982). At each plot, Whittaker laid out a 50-m tape, usually in the upslope direction, along which he established 25 1 3 1 m quadrats on at alternate 1-m intervals. In each quadrat, he counted stems of each species and recorded the species intercepted by each quadrat corner. By summing for each species how many of the 25 quadrat corners it intercepted, he obtained an estimate of percent cover for that species in that plot (25 quadrats 3 4 corners ¼ 100). Within the whole 50 3 20 m plot centered on the tape, he counted tree individuals by diameter at breast height (dbh) classes and species, and shrub individuals by species. He does not appear to have marked, mapped, or returned to these plots (Whittaker 1960; R. H. Whittaker, unpublished data). His data are in the Cornell University Library, Division of Rare and Manuscript Collections. Each plot is described by a plot number, substrate, road or trail, elevation, slope and aspect (e.g., 268, serpentine, Wimer Rd., 2400 0 , E 258). The precision was 308 of aspect (i.e., ENE, WSW) and 30.5 m (100 feet) of elevation. Data for each plot include: numbers of herb individuals by species, percent cover of herbs by species (both of these from summing across the 25 1-m2 quadrats), and numbers of shrub and tree individuals in the 50 3 20 m plot by species. Data on individual quadrats are absent. He deposited voucher specimens in the Ownbey Herbarium at Washington State University, Pullman, Washington, USA. 3611 Present-day data collection We entered Whittaker’s data into a database with herb count, herb cover, and shrub and tree counts, each by species and plot number. We updated species names using the Jepson Interchange (available online).5 The severe Biscuit Fire of 2002 burned Whittaker’s entire gabbro study area at York Butte in the Kalmiopsis Wilderness, but very little of his serpentine study areas at Eight Dollar Mountain, Josephine Mountain, Tennessee Pass, Rough and Ready Creek, and Wimer Road, and none of his diorite sites. However, most of his diorite sites on the Siskiyou National Forest were logged beginning in 1952. In the vicinities of Grayback Campground, Caves Creek Campground, Caves Highway, and Oregon Caves National Monument, we were able to find 53 unlogged Whittaker diorite sites at elevations comparable to those of his 55 serpentine sites (i.e., 400–1200 m). To locate sample plots as close as possible to Whittaker’s (e.g., his plot number 268), we followed the same road or trail on the same substrate (e.g., Wimer Road, serpentine), stopped at the same elevation (e.g., 2400 0 or 702 m), and found the nearest place with the same slope and aspect (e.g., 258 E), using a global positioning system (GPS), topographic maps, and clinometer. Like Whittaker, we avoided disturbances and openings. While the lack of exact plot locations undoubtably adds some random error/uncertainty to data comparisons, we feel our method for establishing resampling plots is free of bias. In May–June 2007, we sampled 55 plots representing all of Whittaker’s serpentine plots, from 410–1140 m elevation. In June–August 2007, we sampled 53 plots representing a subset of Whittaker’s diorite plots that were chosen because they were not logged and matched the serpentine plots in elevation (500–1200 m), so that elevational differences would not confound the substrate difference. We followed Whittaker’s sampling methods exactly, except that we revisited our sites approximately one month later to look for new herb species. For the purposes of this paper, we use the herb percent cover data obtained from the corners of the 25 quadrats and the shrub and tree counts from the 20 3 50 m plot (described above) because these methods are all repeatable by multiple observers. To reconcile identity questions, we examined Whittaker’s voucher specimens at the Ownbey Herbarium in November 2007. For additional conservatism, we used only those species found by both Whittaker and us and eliminated unidentified morphospecies. Because Whittaker recorded grass cover as ‘‘unknown grass,’’ but later identified the grass species present in each plot, we eliminated grass species from analyses dependent on species identity, but retained them for analyses comparing responses of groups (i.e., life forms). 5 hucjeps.berkeley.edu/interchange.htmli 3612 ELLEN I. DAMSCHEN ET AL. Species traits To compare changes in different groups of species, we classified species as belonging to families or genera of northern (Arcto-Tertiary) or southern (Madro-Tertiary, California Floristic Province, or desert) biogeographic affinities, using Raven and Axelrod (1978); see Harrison and Grace [2007] and Ackerly [2003, 2009] for a full discussion of these categories). We also classified species as being either at or not at their northern and southern range limits in the Klamath-Siskiyou region using the USDA Plants Database (USDA 2008). (For this purpose, we defined the Klamath-Siskiyou region as Josephine, Jackson, and Curry Counties, Oregon, and Del Norte, Siskiyou, Humboldt, Trinity, and Shasta Counties, California.) Serpentine endemism was evaluated using the criteria of Safford et al. (2005); based on a literature review, endemics were defined as species with scores of 4.5 on a 6-point scale. Change in widespread species (those without southern or northern range limits in our study region) was compared to changes in species near their latitudinal range limits on both soil types. On serpentine soils, we compared the change in serpentine endemics (species with serpentine scores 4.5) to soil generalists (species with serpentine scores ,4.5). Note that we were unable to classify grasses because Whittaker lumped all grass species into a single group. A list of all study species and their traits can be found in Appendix C. Analyses In order to test our predictions by comparing groups of species with particular traits, we performed two sets of analyses for each comparison of interest. First, we used a nonparametric PERMANOVA (Anderson 2001) with the summed relative cover values of species in the different trait groups as multiple response variables. Year, soil type, and their interactions were included as fixed effects and plot identity as a random effect. We used Euclidean distance measures on log-transformed data. Other transformations and distance measures yielded similar results. We followed significant multivariate non-parametric analyses with univariate models in order to evaluate directionality of responses and differences in the degree of change among species groups and soil types. In this case, species trait categories were used as a predictor variable in addition to year, soil type (fixed effects), and plot identity (random effect). PERMANOVAs were performed with Primer v. 6 with PERMANOVAþ (Clarke and Gorley 2006). SAS version 9.1.3 (SAS Institute 2007) was used for the univariate models. Detailed descriptions of statistical models and their results are presented in Appendix D. For comparisons of forbs and grasses, raw percent cover per plot was used as the response variable of interest. For the univariate model, we used a generalized linear mixed model with a Poisson distribution and log link function. For comparisons of species with northern vs. southern biogeographic affinties, species with their Ecology, Vol. 91, No. 12 range limits in our study region vs. widespread species, and serpentine endemics vs. generalist species, we used relative percent cover as our response variable of interest. In these cases, our univariate models were generalized linear mixed models with binomial distributions and logit link functions. To assess whether species richness changed over time and if soil type altered the degree of change, we used a generalized linear mixed model with a Poisson distribution and log link function. Because Whittaker did not identify grasses to species, we analyzed only the species richness of forbs with year, soil type, and their interaction (fixed effects) and plot location (random effect) as predictor variables. To test whether species composition had changed over time to more strongly resemble the species composition of warm south-facing sites we performed ordinations using PC-ORD v. 4.14 (McCune and Mefford 1999). We ordinated the herb and tree communities separately. We did not ordinate the shrub data because Whittaker did not count individuals of three shrubs he described as being among the most common on serpentine (Garrya buxifolia, Lithocarpus densiflorus var. echioides, and Quercus vaccinifolia), recording them only as present or absent. We also used separate ordinations for the strongly differing communities on serpentine and diorite soils, but we combined the 1950 and 2007 data in each ordination. We ordinated sites with non-metric multidimensional (NMS) ordination (McCune and Grace 2002), excluding those species found in less than 5% of samples. NMS is a computationally intensive technique that searches iteratively for the best position of n entities with p attributes on k axes that minimizes ‘‘stress,’’ defined as deviation from monotonicity in the relationship between dissimilarity of entities in the original p-dimensional space and in the reduced k-dimensional space. We used the autopilot mode in PCOrd to search for the optimal dimension reduction (two to six dimensions) using 200 iterations of the analysis. Autopilot mode is an algorithm in PC-ORD that assists in choosing the best solution in each dimensionality and testing for significance; all options are set automatically (maximum number of iterations, instability criterion, starting number of axes, number of real runs, number of randomized runs), except for the distance metric, which must be selected by the user (McCune and Mefford 1999, McCune and Grace 2002). Significance was evaluated by comparing stress reduction to that found in a random matrix using Monte Carlo permutation tests. We rotated Axis 1 of each ordination to maximize its correlation with Whittaker’s topographic moisture gradient, and tested for significant differences in mean Axis 1 scores between sites in 1950 and sites in 2007 using both conventional test procedures and Markov chain Monte Carlo methods (Gelman and Hill 2007). A positive change in Axis 1 score would indicate that December 2010 ENDEMIC-RICH FLORA AND CLIMATE CHANGE 3613 FIG. 1. Changes in cover of forbs and grasses. Total percent forb and grass cover per plot decreased over time. Error bars represent 95% confidence limits. Lowercase letters indicate significant differences (P 0.05) among groups across both panels (A and B). See Methods and Appendix D for full statistical methods and results. community composition has changed over time in the same direction that composition changes over space from mesic (cooler, moister) to xeric (warmer, drier) slopes. To evaluate corresponding changes in shrubs and trees, we used generalized linear mixed models with a Poisson distribution and log link function. Soil type and year were used as fixed effects and plot location as a random effect. Separate models were run for the number of shrubs, number of trees, number of hardwood trees, and number of coniferous trees per plot. For analyses of hardwood trees, only plots that had hardwood trees present in one or both time periods were included. species near their northern latitudinal limits in the study region on diorite soils and of regional endemics on serpentine soils also declined (Fig. 5). In contrast, widely distributed species whose range limits are not in the Klamath-Siskiyous and species with their southern latitudinal range limits in the study region showed no change in relative cover on either soil type (Fig. 5). Few exotic herb species were found in either time period (1 in 1950, 7 in 2007), and annual herb species were also relatively uncommon (12 in 1950 and 17 in 2007). No exotic herbs had cover values of .0% (i.e., RESULTS Changes in species abundance and richness Total herb cover was sharply lower in 2007 than in 1950 on both diorite and serpentine (Fig. 1). This decline in herb cover was greater on serpentine than on diorite. On both soils, the decline in cover was much greater for forbs than grasses. Mean numbers of herb species at each site (alpha diversity) likewise declined (Fig. 2), although the total numbers of herb species at all sites combined (gamma diversity) did not decline (117 vs. 122 species in 1950 and 2007, respectively). The decline in species richness was greater on serpentine than diorite soils. Relative cover (i.e., the cover by a group divided by total cover in a plot) of species belonging to taxa of northern biogeographic affinity declined on both soil types, while the relative cover of species with southern biogeographic affinity increased on diorite and showed no change on serpentine (Fig. 3). Relative cover of edaphic endemic forbs declined more than generalist forbs on serpentine soils (Fig. 4). The relative cover of FIG. 2. Forb species richness per plot decreased over time, and this decline was smaller on diorite than on serpentine soils. Lowercase letters indicate significant differences (P 0.05) among groups. Error bars represent 95% confidence limits. See Methods and Appendix D for full statistical methods and results. 3614 ELLEN I. DAMSCHEN ET AL. Ecology, Vol. 91, No. 12 FIG. 3. Changes in species with northern and southern biogeographic affinities. The relative percent cover out of the total herb cover per plot for species belonging to taxa of northern biogeographic affinities declined over time on (A) diorite and (B) serpentine soils, while the relative percent cover of species belonging to higher taxa with southern biogeographic affinities increased on diorite and did not change on serpentine. Error bars represent 95% confidence limits. Lowercase letters indicate significant differences (P 0.05) among groups across both panels (A) and (B). See Methods and Appendix D for full statistical methods and results. they were present but never intercepted a quadrat corner). On serpentine, the number of shrubs increased and the number of tree individuals did not change. On diorite, the numbers of shrub and tree individuals decreased over time; declines were most evident in hardwood trees, while coniferous trees increased (Fig. 6). Detailed statistical results for all of these analyses can be found in Appendix D. Changes in community composition All four ordinations (diorite herbs, serpentine herbs, diorite trees, and serpentine trees) caused significant reductions in stress within the dissimilarity matrices compared to randomized data based on Monte Carlo tests. Minimum stress values obtained were 19.1%, 21.3%, 9.8%, and 12.7%, respectively. Herb community composition at both diorite and serpentine sites shifted toward significantly higher Axis 1 scores in 2007 compared to 1950 (Fig. 7A), meaning that communities in 2007 included greater relative cover by species characteristic of warm south-facing locations, and lower relative cover by species characteristic of cool north-facing locations, than the communities at the corresponding locations in 1950. This was not true for trees (Fig. 7B). These results were consistent based on both conventional frequentist tests and credible intervals produced using Markov chain Monte Carlo methods (Gelman and Hill 2007). Ordination plots can be found in Appendix E. Such community-level shifts in herbs could arise because species peak abundances are now found on cooler slopes than in the past (i.e., sites that are cooler within any one time period, such as more northerly slopes), and thus sites are left with arrays of species more characteristic of warm sites (i.e., sites that are warmer within any one time period, such as more southerly slopes). We found evidence for this in diorite herbs, for which peak abundances (abundance-weighted mean TMG positions) significantly shifted toward cooler microsites (TMG score change ¼ 0.10 6 0.04 [mean 6 SE], t1,26 ¼ 2.34, P ¼ 0.027). This shift was generated predominantly by differential losses of species across cool and warm sites, as opposed to increases in abundance on cool sites; overall, 85% of species on diorite soils decreased in total abundance. On serpentine, the peak distributions for individual species did not shift along the topographic moisture gradient (abundance-weighted TMG score change ¼0.02 6 0.04, t1,43 ¼ 0.52, P ¼ 0.603). Instead, the shift toward ‘‘warmer’’ community composition appears to be associated with the disproportionate loss of the abundance of forbs relative to grasses (Fig. 1). FIG. 4. Changes in serpentine endemics and generalists. The relative percent cover of species in each plot that are endemic to serpentine declined over time while generalists did not change over time. Lowercase letters represent statistically significant differences (P 0.05) among groups. Error bars represent 95% confidence limits. See Methods and Appendix D for full statistical methods and results. December 2010 ENDEMIC-RICH FLORA AND CLIMATE CHANGE FIG. 5. Changes in species with range limits in the study region vs. widespread species. The relative percent cover per plot of widespread herbs on (A) diorite and (E) serpentine soils did not change over time. Species with northern range limits in the study region on (B) diorite soils declined over time but showed no change on (F) serpentine. Species with their southern range limits in the study region showed no change on either (C) diorite or (G) serpentine soils. Regional endemics did not change on (D) diorite but significantly declined on (H) serpentine over time. Error bars represent 95% confidence limits; n.s., not significant. See Methods and Appendix D for full statistical methods and results. 3615 FIG. 6. Shrub and tree change over time. The number of shrubs per plot has declined on (A) diorite but has increased on (E) serpentine. The number of trees per plot on (B) diorite has decreased over time but has not changed on (F) serpentine. Hardwood trees have (C) decreased on diorite and (G) serpentine. Coniferous trees have increased on (D) diorite but have decreased on (H) serpentine. Error bars represent 95% confidence limits. See Methods and Appendix D for full statistical methods and results. DISCUSSION Our results indicate that herb communities in the Klamath-Siskiyous have dramatically declined in overall abundance and changed in species composition over the past 57 years. Declines have been strongest in the most unusual elements of this flora, including species that are found on serpentine soil and are endemic to the region, and species that are endemic to serpentine soils. 3616 ELLEN I. DAMSCHEN ET AL. FIG. 7. Changes in community composition. For the (A) herb community, differences in Axis 1 ordination scores (i.e., the topographic moisture gradient) were calculated by subtracting the 1950 score from the 2007 score. Positive differences were significantly different from zero on both diorite and serpentine soils, indicating that communities today are composed of more xeric-associated species than they were in 1950. For the (B) tree community, there were no significant shifts, indicating that tree communities have neither become more mesic nor more xeric over time on either soil type. Medians and 95% percentiles are shown for each soil type. Climatic warming Vegetation change in response to climatic warming is implicated by two aspects of our results. First, as we expected, declines in herb cover were strong in species belonging to families and genera of northern (ArctoTertiary) biogeographic origins, and much weaker in those belonging to families and genera of southern (Madro-Tertiary) biogeographic origins (Raven and Axelrod 1978). These two groups have been shown to have opposing responses to climatic variation over both time (Valiente-Banuet et al. 2006) and space (Harrison and Grace 2007, Ackerly 2009). In woody species, it has been shown that northern-origin taxa are characterized by broad, thin leaves and other adaptations to cooler and moister habitats, while southern-origin taxa tend to show the opposite sets of traits (Ackerly 2003, 2009). The second source of evidence for climatic warming is that, again as predicted, the overall shifts in herb community composition on both serpentine and diorite Ecology, Vol. 91, No. 12 soils were in the warmer direction along Whittaker’s topographic moisture gradient. In other words, the herb species composition of sites in 2007, compared with that of the corresponding sites in 1950, has changed to more strongly resemble the species composition of a warm south-facing slope. Such a shift can arise both from the differential declines of species characteristic of cool north-facing slopes (such as the Raven-Axelrod ‘‘northern’’ species), and from losses of populations toward the warmer ends of species’ local topographic distributions. The lack of such shifts in trees is not surprising, given their slower population dynamics, and this lack of change in trees also suggests that our herb community results were not caused by biased site selection. We found declines in species with their northern range limits in the Klamath-Siskiyou region, and no relative change in those with southern limits in this region, contrasting with the expected pattern under a warming scenario. While we cannot fully explain this result, we suspect that one contributing factor is the extreme topography and complex biogeographic history of this region. When species reach their range limits in this region, it may be more because of physical barriers or for other historical reasons than because they reach their climatic limits within a smoothly varying north-to-south gradient of temperature and moisture. If this is true, or if locally adapted climatic ecotypes are prevalent, then regional range limits will not be good predictors of climatic tolerances. Susceptibility of the endemic-rich serpentine flora vs. normal soils The community-level shift to a warmer species composition was just as strong in the herb flora of serpentine soils as in that of diorite soils. Furthermore, within the serpentine herb flora, edaphic endemic species declined more than more widespread species. The one striking exception was that grasses, which provide a substantial amount of herb cover on serpentine but not on diorite, appeared relatively resistant to the changes that affected other herbs (unfortunately we could not examine grass responses in detail because we lacked species-specific information from Whittaker). Our results appear inconsistent with those of Grime et al. (2000, 2008), who found lesser sensitivity to experimental warming and drought in a nutrient-poor ‘ancient’ limestone grassland than a more disturbed and fertile one, and who concluded that nutrient-poor ecosystems are secure refuges for biodiversity in the face of climate change unless they are also subjected to land-use change. Moreover, our results also contrast with those of a paleoecological study, in which Briles (2008) found a lesser degree of centennial-to-millenial fluctuation in the dominant woody vegetation on serpentine than granite soils in the Klamath Mountains, California, USA over the past 15 000 years. One possible explanation for the discrepancy between our results and these previous studies is that we December 2010 ENDEMIC-RICH FLORA AND CLIMATE CHANGE 3617 examined herbaceous understories beneath woody canopies. While canopies are dense and continuous on diorite soils, they are much more open and patchy on serpentine, potentially leading to less buffering of ground surface temperatures on serpentine (consistent with this, we found greater north-south slope differences in near-surface temperatures on serpentine than diorite; E. Damschen and S. Harrison, unpublished data). Whatever the explanation, our results suggest that complacency is unwise when considering the future of special-soil floras under climate change, especially those that occur on isolated outcrops within narrow elevational ranges. Topographic shifts are a possible means by which species can be buffered against climate change and perhaps survive without long-distance dispersal (e.g., Weiss and Weiss 1998, Loarie et al. 2009). However, we found little evidence of this buffering effect in our study, since the majority of herb species (38 of 42 on diorite and 75 of 79 on serpentine) declined in cover on both the cooler and warmer halves of the topographic gradient. Our study stands as a warning that there may be a substantial lag time in species responses, such that even at the microsite level, declines in unfavorable locations long precede increases in newly favorable ones. Other factors contributing to change Conclusions Livestock grazing and exotic species do not appear to be important influences in our study region, and we avoided logged sites, but fire suppression is another potential source of vegetation change. Fire has been excluded from our study areas since the early 1900s, while return intervals were previously 12–19 years (Agee 1991, Skinner 1995). Our diorite sites might be expected to be in the canopy closure stage of succession, characterized by conifer dominance, stable tree abundance, and shady understories (Taylor and Skinner 2003, Odion et al. 2004, Jules et al. 2008). Increased shading is consistent with some of the changes we observed, including the decline in hardwoods and increase in conifers on diorite and the decline in herb cover on both soils. However, increased shading does not explain the relative decline in herbs of northern biogeographic affinity, the community shifts to warmer species composition, or the shifts of species peak abundances to cooler topographic positions on diorite. Thus, our results suggest that the effects of a warming climate have been strong enough to overcome any potential ameliorating effect of the shadier conditions created by fire suppression. In the woody community on serpentine, shrubs increased and conifers decreased. We know little about the possible causes of these changes, though we can speculate on possible roles for fire suppression and occasional small-scale harvesting of conifers for timber. It is also interesting to note that Briles (2008) found declines in trees (notably Pinus jeffreyi ) and increases in shrubs (notably Quercus vaccinifolia) on serpentine during early Holocene warming. Random variation in rainfall is unlikely to explain the declines in herb cover we observed. The years that Whittaker sampled (1950) had 73%, 76%, and 63% of the 105-year mean of growing-season (February–June) rainfall, while 2007 had 97% of the mean amount (data from the National Oceanic and Atmospheric Administration for Grants Pass, Oregon; available online).6 Our study demonstrates a paradox: regions that have acted as climatic refugia in the past, in part because of their rugged topography and variety of available microclimates, may contain a disproportionate number of narrowly distributed species (Ohlemuller et al. 2008). Thus, such regions may also show elevated rates of extinction under rapid modern climatic warming. It also may be unrealistic to expect lesser changes in stresstolerant species such as our serpentine endemics, since these species already occur in more abiotically stressful locations. While managed relocation (i.e., assisted colonization, assisted migration) remains controversial (McLachlan et al. 2007, Davidson and Simkanin 2008, Hoegh-Guldberg et al. 2008, Huang 2008), we suggest that narrowly distributed edaphic endemics should be considered high-priority candidates if and when such intervention is contemplated. 6 hhttp://www.wrcc.dri.edui The role of topography under global climate change ACKNOWLEDGMENTS L. L. Olsvig-Whittaker and the Cornell University Library’s Division of Rare and Manuscript Collections provided access to Robert Whittaker’s data. Field and data entry assistance were provided by M. Brown, T. Elder, K. Fuccillo, C. Garnier, J. Hansford, T. Hoang, F. Hrusa, M. Jules, A. King, K. Kostelnik, R. Mack, K. Moore, T. Talty, and K. Torres. Valuable discussions and manuscript comments were provided by D. Ackerly, H. Cornell, N. Haddad, E. Jules, D. Levey, D. Odion, J. Orrock, R. Peet, J. Roth, N. Sanders, M. Schwartz, A. Storfer, J. Tewksbury, T. 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VegetatioC97–122. Whittaker, R. H. 1960. Vegetation of the Siskiyou Mountains, Oregon and California. Ecological Monographs 30:279–338. APPENDIX A A figure showing average summer temperatures over time near the study region (Ecological Archives E091-254-A1). APPENDIX B A figure demonstrating Whittaker’s topographic moisture gradient (TMG) (Ecological Archives E091-254-A2). APPENDIX C A table of species and traits used in the analyses (Ecological Archives E091-254-A3). APPENDIX D Tables presenting statistical results for data analyses (Ecological Archives E091-254-A4). APPENDIX E Figures of herb community ordination for diorite and serpentine soils (Ecological Archives E091-254-A5).